Self-splicing group I intron in cyanobacterial initiator methionine tRNA: evidence for lateral transfer of introns in bacteria.

Biniszkiewicz, Detlev; Cesnaviciene, E.; Shub, David A.

doi:10.1002/j.1460-2075.1994.tb06785.x

Cited by 72 publications

(85 citation statements)

References 21 publications

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“…This is supported by the observed accumulation of tRNA Tyr processing intermediates when expression of TbTrl1 is down-regulated. As for TbRtcB, its function is not currently clear in T. brucei; however, eubacterial genomes harbor RtcB genes despite encoding self-splicing intron-containing tRNAs (Kuhsel et al 1990;Reinhold and Shub 1992;Biniszkiewicz et al 1994). In these cases, RtcB is involved in RNA repair as previously proposed for E. coli (Tanaka and Schuman 2011) and the same may be true of the T. brucei homolog.…”

Section: Discussionmentioning

confidence: 79%

The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNA^Tyr

Lopes

Silveira

Eitler

et al. 2016

RNA

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Trypanosoma brucei, the etiologic agent of sleeping sickness, encodes a single intron-containing tRNA, tRNA Tyr , and splicing is essential for its viability. In Archaea and Eukarya, tRNA splicing requires a series of enzymatic steps that begin with intron cleavage by a tRNA-splicing endonuclease and culminates with joining the resulting tRNA exons by a splicing tRNA ligase.Here we explored the function of TbTrl1, the T. brucei homolog of the yeast Trl1 tRNA ligase. We used a combination of RNA interference and molecular biology approaches to show that down-regulation of TbTrl1 expression leads to accumulation of intron-containing tRNA Tyr and a concomitant growth arrest at the G1 phase. These defects were efficiently rescued by expression of an "intronless" version of tRNA Tyr in the same RNAi cell line. Taken together, these experiments highlight the crucial importance of the TbTrl1 for tRNA Tyr maturation and viability, while revealing tRNA splicing as its only essential function.

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Section: Discussionmentioning

confidence: 79%

The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNA^Tyr

Lopes

Silveira

Eitler

et al. 2016

RNA

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“…Cyanobacterial populations have a number of advantages for such analyses : they have a cosmopolitan distribution ; they dominate the microbial populations of many extreme environments ; their colonies are often conspicuous and may assume macrophytic proportions ; colonies of what appear to be morphologically identical forms occur in geographically isolated environments ; growths, often attributed to a ' monospecific ' population, may cover many square kilometres ; and cyanobacteria have a D. Wright and others fossil record. Of those genetic markers that may resolve clusters and groupings within taxa below the level of genus, group I intron sequences have been investigated in a broad range of eubacterial taxa (Biniszkiewicz et al, 1994 ;Paquin et al, 1997Paquin et al, , 1999Edgell et al, 2000). In this study, we focussed on a large set of desiccated samples of free-living Nostoc for which detailed records were available of time and place of origin and taxonomic assignment.…”

Section: Discussionmentioning

confidence: 99%

Form species Nostoc commune (Cyanobacteria).

Wright¹,

Prickett²,

Helm³

et al. 2001

International Journal of Systematic and Evolutionary Microbiology

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The form species concept for the Cyanobacteria was evaluated using a comprehensive set of Nostoc samples that were collected during the past two centuries, from all continents, including regions from the Tropics to the Poles. Phylogenies were constructed based upon the conserved regions of tRNA Leu (UAA) group I intron DNA sequences. Thirty-four forms contained a tRNA Leu (UAA) intron of 284 nt. These 284-nt introns contained 200 nt of conserved sequence that, in most cases, shared 100 % sequence identity, they had three variable regions (I, II and III) amounting to 84 nt, contained no hypervariable region and formed a discrete cluster in phylogenetic analysis. These forms represented 31 independent populations in both hemispheres and constitute examples of form species Nostoc commune. Multiple introns were obtained from several of the populations. Ten populations contained introns of 287-340 nt with a hypervariable region, 8 to 59 nt in length, located between variable regions I and II. Alignments identified 15 examples where 5'-AAAAUCC-3' occurred at the hypervariable region-variable region II boundary ; this sequence is identical to the conserved sequence at the 3' intron-exon boundary (splice site) within the tRNA Leu (UAA) gene. The possibility that hypervariable regions were removed from the primary intron through secondary splicing was tested in vitro but proved to be negative under the experimental conditions used. Shared morphologies of genetically different strains, dissimilar morphologies in strains that share identical genetic markers, incorrect naming of culture collection strains and genetic drift in cultured strains emphasize that the successful delineation of cyanobacterial species requires the application of multiple taxonomic criteria.

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“…The first exception is the tRNA fMet intron of Synechocystis that contains an ORF that potentially codes for a small basic protein not similar to any known endonuclease (6), and the second is a LAGLIDAG endonuclease ORF within the S. negevensis Z T 23S rDNA insertion (21). However, in spite of the tendency for phage introns to encode endonucleases, not all phage introns do, and some appear to have remnants of ORFs, evidenced by the phage T4 nrdB intron (19) and the Bacillus phage ␤22 thymidylate synthase intron (1).…”

Section: Where Are Group I and Ii Introns Found?mentioning

confidence: 99%

Barriers to Intron Promiscuity in Bacteria

2000

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2"The field of bacterial viruses is a fine playground for serious children who ask ambitious questions."Max DelbruckThe first bacterial intron, a self-splicing group I intron, was found to interrupt the thymidylate synthase (td) gene of the Escherichia coli phage T4 (11). The second and third bacterial group I introns were found to interrupt the aerobic (nrdB) and anaerobic (nrdD [initially named sunY]) ribonucleotide reductases of phage T4 (29,90), and another group I intron was soon discovered in the DNA polymerase gene of SPO1, a Bacillus phage (25). From this (admittedly) small sampling of phage genomes, one might have naively expected that group I introns would be abundant in phage or bacterial genomes, especially since subsequent laboratory experiments demonstrated that group I introns could propagate themselves (by a process called homing) throughout populations of intron-minus alleles with near 100% efficiency (5, 68). That a similar homing phenomenon had also been previously demonstrated for a group I intron in the large rRNA gene of yeast mitochondria (34) gave additional support to the notion that group I introns should be able to spread efficiently throughout populations. However, this expected outcome has never been realized in natural phage populations; some phage populations harbor many introns, while other related phage populations are strangely lacking in any introns whatsoever (Table 1). Why do group I introns have an unusual distribution in phage and bacterial genomes, and what potential barriers might exist to prevent their spread?A similar question might be asked of group II introns in bacteria. Much was made of the initial finding of group II introns in bacteria, as their discovery added fuel to the debate concerning the evolutionary origins of eukaryotic spliceosomal introns (22, 70) which have both structural and functional similarities to group II introns (53,79,84). Yet, the number of group II introns in bacteria is small, many of which are inferred only from database matches to reverse transcriptases or maturases encoded within known introns (13,41,73,89), and only two have been shown to splice or be mobile in vivo (48,49,55,80) (Table 2). While group II intron homing is mechanistically distinct from group I intron homing, the principle is similar; group II introns home from intron-containing to intronless alleles. Many elegant biochemical and genetic experiments have unraveled the complexities of bacterial group II intron homing (14,48,49), and based on these results, there seems no a priori reason why group II introns should not be able to spread efficiently through populations of intron-minus alleles. The paucity of bacterial group II introns becomes even more perplexing given the recent demonstration of group II intron transposition to novel chromosomal sites (15). That group II introns are abundant in mitochondrial and chloroplast genomes (52) and present in bacterial genomes but at lower levels (and absent in phages) only adds to the mystery surrounding the lack of group II intro...

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Self-splicing group I intron in cyanobacterial initiator methionine tRNA: evidence for lateral transfer of introns in bacteria.

Cited by 72 publications

References 21 publications

The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNA^Tyr

The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNA^Tyr

Form species Nostoc commune (Cyanobacteria).

Barriers to Intron Promiscuity in Bacteria

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Self-splicing group I intron in cyanobacterial initiator methionine tRNA: evidence for lateral transfer of introns in bacteria.

Cited by 72 publications

References 21 publications

The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNATyr

The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNATyr

Form species Nostoc commune (Cyanobacteria).

Barriers to Intron Promiscuity in Bacteria

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The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNA^Tyr

The essential function of the Trypanosoma brucei Trl1 homolog in procyclic cells is maturation of the intron-containing tRNA^Tyr